Enteroviruses in the pathogenesis of type 1 diabetes

Andreoletti L, Hober D, Hober-Vandenberghe C, Belaich S, Vantyghem MC, Lefebvre J, Wattre P (1997) Detection of coxsackie B virus RNA sequences in whole blood samples from adult patients at the onset of type I diabetes mellitus. J Med Virol 52:121–127 Beck MA, Levander OA, Handy J (2003) Selenium deficiency and viral infection. J Nutr 133:1463S–1467S Cerutis DR, Bruner RH, Thomas DC, Giron DJ (1989) Tropism and histopathology of the D, B, K, and MM variants of encephalomyocarditis virus. J Med Virol 29:63–69 Chapman NM, Kim KS (2008) Persistent coxsackievirus infection: enterovirus persistence in chronic myocarditis and dilated cardiomyopathy. Curr Top Microbiol Immunol 323:275–292 Chapman NM, Kim KS, Drescher KM, Oka K, Tracy S (2008) 5′ terminal deletions in the genome of a coxsackievirus B2 strain occurred naturally in human heart. Virology 375:480–491 Chehadeh W, Kerr-Conte J, Pattou F, Alm G, Lefebvre J, Wattre P, Hober D (2000) Persistent infection of human pancreatic islets by coxsackievirus B is associated with alpha interferon synthesis in beta cells. J Virol 74:10153–10164 Chehadeh W, Weill J, Vantyghem MC, Alm G, Lefebvre J, Wattre P, Hober D (2000) Increased level of interferon-alpha in blood of patients with insulin-dependent diabetes mellitus: relationship with coxsackievirus B infection. J Infect Dis 181:1929–1939 Clements GB, Galbraith DN, Taylor KW (1995) Coxsackie B virus infection and onset of childhood diabetes. Lancet 346:221–223 Craig ME, Howard NJ, Silink M, Rawlinson WD (2003) Reduced frequency of HLA DRB1*03-DQB1*02 in children with type 1 diabetes associated with enterovirus RNA. J Infect Dis 187:1562–1570 Dahlquist GG, Ivarsson S, Lindberg B, Forsgren M (1995) Maternal enteroviral infection during pregnancy as a risk factor for childhood IDDM. A population-based case-control study. Diabetes 44:408–413 Dahlquist GG, Boman JE, Juto P (1999) Enteroviral RNA and IgM antibodies in early pregnancy and risk for childhood-onset IDDM in offspring. Diabetes Care 22:364–365 Dahlquist GG, Forsberg J, Hagenfeldt L, Boman J, Juto P (2004) Increased prevalence of enteroviral RNA in blood spots from newborn children who later developed type 1 diabetes: a population-based case-control study. Diabetes Care 27:285–286 Dotta F, Censini S, van Halteren AG, Marselli L, Masini M, Dionisi S, Mosca F, Boggi U, Muda AO, Prato SD, Elliott JF, Covacci A, Rappuoli R, Roep BO, Marchetti P (2007) Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc Natl Acad Sci USA 104:5115–5120 Dotta F, Fondelli C, Falorni A (2008) Can NK cells be a therapeutic target in human type 1 diabetes? Eur J Immunol 38:2961–2963 Drescher KM, Sosnowska D (2008) Being a mouse in a man’s world: what TMEV has taught us about human disease. Front Biosci 13:3775–3785 Elshebani A, Olsson A, Westman J, Tuvemo T, Korsgren O, Frisk G (2007) Effects on isolated human pancreatic islet cells after infection with strains of enterovirus isolated at clinical presentation of type 1 diabetes. Virus Res 124:193–203 Feuer R, Ruller CM, An N, Tabor-Godwin JM, Rhoades RE, Maciejewski S, Pagarigan RR, Cornell CT, Crocker SJ, Kiosses WB, Pham-Mitchell N, Campbell IL, Whitton JL (2009) Viral persistence and chronic immunopathology in the adult central nervous system following Coxsackievirus infection during the neonatal period. J Virol 83:9356–9369 Filippi CM, Estes EA, Oldham JE, von Herrath MG (2009) Immunoregulatory mechanisms triggered by viral infections protect from type 1 diabetes in mice. J Clin Invest 119:1515–1523 Foulis AK, Farquharson MA, Cameron SO, McGill M, Schonke H, Kandolf R (1990) A search for the presence of the enteroviral capsid protein VP1 in pancreases of patients with type 1 (insulin-dependent) diabetes and pancreases and hearts of infants who died of coxsackieviral myocarditis. Diabetologia 33:290–298 Foulis AK, McGill M, Farquharson MA, Hilton DA (1997) A search for evidence of viral infection in pancreases of newly diagnosed patients with IDDM. Diabetologia 40:53–61 Foy CA, Quirke P, Lewis FA, Futers TS, Bodansky HJ (1995) Detection of common viruses using the polymerase chain reaction to assess levels of viral presence in type 1 (insulin-dependent) diabetic patients. Diabet Med 12:1002–1008 Fuchtenbusch M, Irnstetter A, Jager G, Ziegler AG (2001) No evidence for an association of coxsackie virus infections during pregnancy and early childhood with development of islet autoantibodies in offspring of mothers or fathers with type 1 diabetes. J Autoimmun 17:333–340 Gamble DR, Kinsley ML, FitzGerald MG, Bolton R, Taylor KW (1969) Viral antibodies in diabetes mellitus. Br Med J 3:627–630 Gamble DR, Taylor KW (1969) Seasonal incidence of diabetes mellitus. Br Med J 3:631–633 Gianani R, Putnam A, Still T, Yu L, Miao D, Gill RG, Beilke J, Supon P, Valentine A, Iveson A, Dunn S, Eisenbarth GS, Hutton J, Gottlieb P, Wiseman A (2006) Initial results of screening of non-diabetic organ donors for expression of islet autoantibodies. J Clin Endocrinol Metab 91:1855–1861 Gladisch R, Hofmann W, Waldherr R (1976) Myocarditis and insulitis following coxsackie virus infection. Z Kardiol 65:837–849 Graves PM, Rotbart HA, Nix WA, Pallansch MA, Erlich HA, Norris JM, Hoffman M, Eisenbarth GS, Rewers M (2003) Prospective study of enteroviral infections and development of beta-cell autoimmunity. Diabetes autoimmunity study in the young (DAISY). Diabetes Res Clin Pract 59:51–61 Harkonen T, Puolakkainen M, Sarvas M, Airaksinen U, Hovi T, Roivainen M (2000) Picornavirus proteins share antigenic determinants with heat shock proteins 60/65. J Med Virol 62:383–391 Harkonen T, Lankinen H, Davydova B, Hovi T, Roivainen M (2002) Enterovirus infection can induce immune responses that cross-react with beta-cell autoantigen tyrosine phosphatase IA-2/IAR. J Med Virol 66:340–350 Harkonen T, Paananen A, Lankinen H, Hovi T, Vaarala O, Roivainen M (2003) Enterovirus infection may induce humoral immune response reacting with islet cell autoantigens in humans. J Med Virol 69:426–440 Hermitte L, Vialettes B, Naquet P, Atlan C, Payan MJ, Vague P (1990) Paradoxical lessening of autoimmune processes in non-obese diabetic mice after infection with the diabetogenic variant of encephalomyocarditis virus. Eur J Immunol 20:1297–1303 Hiltunen M, Hyoty H, Knip M, Ilonen J, Reijonen H, Vahasalo P, Roivainen M, Lonnrot M, Leinikki P, Hovi T, Akerblom HK (1997) Islet cell antibody seroconversion in children is temporally associated with enterovirus infections. Childhood Diabetes in Finland (DiMe) Study Group. J Infect Dis 175:554–560 Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N (1998) Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med 4:781–785 Huhn MH, McCartney SA, Lind K, Svedin E, Colonna M, Flodstrom-Tullberg M Melanoma differentiation-associated protein-5 (MDA-5) limits early viral replication but is not essential for the induction of type 1 interferons after Coxsackievirus infection. Virology Hyoty H, Hiltunen M, Knip M, Laakkonen M, Vahasalo P, Karjalainen J, Koskela P, Roivainen M, Leinikki P, Hovi T et al (1995) A prospective study of the role of coxsackie B and other enterovirus infections in the pathogenesis of IDDM. Childhood Diabetes in Finland (DiMe) Study Group. Diabetes 44:652–657 Hyoty H (2004) Environmental causes: viral causes. Endocrinol Metab Clin North Am 33:27–44, viii Iwasaki T, Monma N, Satodate R, Kawana R, Kurata T (1985) An immunofluorescent study of generalized Coxsackie virus B3 infection in a newborn infant. Acta Pathol Jpn 35:741–748 Jun HS, Kang Y, Notkins AL, Yoon JW (1997) Gain or loss of diabetogenicity resulting from a single point mutation in recombinant encephalomyocarditis virus. J Virol 71:9782–9785 Kawashima H, Ihara T, Ioi H, Oana S, Sato S, Kato N, Takami T, Kashiwagi Y, Takekuma K, Hoshika A, Mori T (2004) Enterovirus-related type 1 diabetes mellitus and antibodies to glutamic acid decarboxylase in Japan. J Infect 49:147–151 Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA (2006) Enterovirus surveillance—United States, 1970–2005. MMWR Surveill Summ 55:1–20 Kim KS, Tracy S, Tapprich W, Bailey J, Lee CK, Kim K, Barry WH, Chapman NM (2005) 5′-Terminal deletions occur in coxsackievirus B3 during replication in murine hearts and cardiac myocyte cultures and correlate with encapsidation of negative-strand viral RNA. J Virol 79:7024–7041 Kruppenbacher JP, Mertens T, Muntefering H, Eggers HJ (1985) Encephalomyocarditis virus and diabetes mellitus: studies on virus mutants in susceptible and non-susceptible mice. J Gen Virol 66(Pt 4):727–732 Lonnrot M, Korpela K, Knip M, Ilonen J, Simell O, Korhonen S, Savola K, Muona P, Simell T, Koskela P, Hyoty H (2000) Enterovirus infection as a risk factor for beta-cell autoimmunity in a prospectively observed birth cohort: the Finnish Diabetes Prediction and Prevention Study. Diabetes 49:1314–1318 Lonnrot M, Salminen K, Knip M, Savola K, Kulmala P, Leinikki P, Hyypia T, Akerblom HK, Hyoty H (2000) Enterovirus RNA in serum is a risk factor for beta-cell autoimmunity and clinical type 1 diabetes: a prospective study. Childhood Diabetes in Finland (DiMe) Study Group. J Med Virol 61:214–220 Makela M, Vaarala O, Hermann R, Salminen K, Vahlberg T, Veijola R, Hyoty H, Knip M, Simell O, Ilonen J (2006) Enteral virus infections in early childhood and an enhanced type 1 diabetes-associated antibody response to dietary insulin. J Autoimmun 27:54–61 Moya-Suri V, Schlosser M, Zimmermann K, Rjasanowski I, Gurtler L, Mentel R (2005) Enterovirus RNA sequences in sera of schoolchildren in the general population and their association with type 1-diabetes-associated autoantibodies. J Med Microbiol 54:879–883 Nairn C, Galbraith DN, Taylor KW, Clements GB (1999) Enterovirus variants in the serum of children at the onset of Type 1 diabetes mellitus. Diabet Med 16:509–513 Nejentsev S, Walker N, Riches D, Egholm M, Todd JA (2009) Rare variants of IFIH1, a gene implicated in antiviral responses, protect against type 1 diabetes. Science 324:387–389 Oikarinen M, Tauriainen S, Honkanen T, Oikarinen S, Vuori K, Kaukinen K, Rantala I, Maki M, Hyoty H (2008) Detection of enteroviruses in the intestine of type 1 diabetic patients. Clin Exp Immunol 151:71–75 Oikarinen M, Tauriainen S, Honkanen T, Vuori K, Karhunen P, Vasama-Nolvi C, Oikarinen S, Verbeke C, Blair GE, Rantala I, Ilonen J, Simell O, Knip M, Hyoty H (2008) Analysis of pancreas tissue in a child positive for islet cell antibodies. Diabetologia 51:1796–1802 Parkkonen P, Hyoty H, Koskinen L, Leinikki P (1992) Mumps virus infects beta cells in human fetal islet cell cultures upregulating the expression of HLA class I molecules. Diabetologia 35:63–69 Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG (2009) The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia 52:1143–1151 Richer MJ, Horwitz MS (2009) Coxsackievirus infection as an environmental factor in the etiology of type 1 diabetes. Autoimmun Rev 8:611–615 Roivainen M, Ylipaasto P, Savolainen C, Galama J, Hovi T, Otonkoski T (2002) Functional impairment and killing of human beta cells by enteroviruses: the capacity is shared by a wide range of serotypes, but the extent is a characteristic of individual virus strains. Diabetologia 45:693–702 Ross ME, Onodera T, Brown KS, Notkins AL (1976) Virus-induced diabetes mellitus. IV. Genetic and environmental factors influencing the development of diabetes after infection with the M variant of encephalomyocarditis virus. Diabetes 25:190–197 Sadeharju K, Lonnrot M, Kimpimaki T, Savola K, Erkkila S, Kalliokoski T, Savolainen P, Koskela P, Ilonen J, Simell O, Knip M, Hyoty H (2001) Enterovirus antibody levels during the first two years of life in prediabetic autoantibody-positive children. Diabetologia 44:818–823 Sadeharju K, Hamalainen AM, Knip M, Lonnrot M, Koskela P, Virtanen SM, Ilonen J, Akerblom HK, Hyoty H (2003) Enterovirus infections as a risk factor for type I diabetes: virus analyses in a dietary intervention trial. Clin Exp Immunol 132:271–277 Sadeharju K, Knip M, Hiltunen M, Akerblom HK, Hyoty H (2003) The HLA-DR phenotype modulates the humoral immune response to enterovirus antigens. Diabetologia 46:1100–1105 Sadeharju K, Knip M, Virtanen SM, Savilahti E, Tauriainen S, Koskela P, Akerblom HK, Hyoty H (2007) Maternal antibodies in breast milk protect the child from enterovirus infections. Pediatrics 119:941–946 Salminen K, Sadeharju K, Lonnrot M, Vahasalo P, Kupila A, Korhonen S, Ilonen J, Simell O, Knip M, Hyoty H (2003) Enterovirus infections are associated with the induction of beta-cell autoimmunity in a prospective birth cohort study. J Med Virol 69:91–98 Salminen KK, Vuorinen T, Oikarinen S, Helminen M, Simell S, Knip M, Ilonen J, Simell O, Hyoty H (2004) Isolation of enterovirus strains from children with preclinical Type 1 diabetes. Diabet Med 21:156–164 Sauter P, Hober D (2009) Mechanisms and results of the antibody-dependent enhancement of viral infections and role in the pathogenesis of coxsackievirus B-induced diseases. Microbes Infect 11:443–451 Sayama K, Imagawa A, Okita K, Uno S, Moriwaki M, Kozawa J, Iwahashi H, Yamagata K, Tamura S, Matsuzawa Y, Hanafusa T, Miyagawa J, Shimomura I (2005) Pancreatic beta and alpha cells are both decreased in patients with fulminant type 1 diabetes: a morphometrical assessment. Diabetologia 48:1560–1564 Seiskari T, Kondrashova A, Viskari H, Kaila M, Haapala AM, Aittoniemi J, Virta M, Hurme M, Uibo R, Knip M, Hyoty H (2007) Allergic sensitization and microbial load—a comparison between Finland and Russian Karelia. Clin Exp Immunol 148:47–52 Shibasaki S, Imagawa A, Tauriainen S, Iino M, Oikarinen M, Abiru H, Tamaki K, Seino H, Nishi K, Takase I, Okada Y, Uno S, Murase-Mishiba Y, Terasaki J, Makino H, Shimomura I, Hyoty H, Hanafusa T (2009) Expression of toll-like receptors in the pancreas of recent-onset fulminant type 1 diabetes. Endocr J Shigemoto T, Kageyama M, Hirai R, Zheng J, Yoneyama M, Fujita T (2009) Identification of loss of function mutations in human genes encoding RIG-I and MDA5: implications for resistance to type I diabetes. J Biol Chem 284:13348–13354 Smyth DJ, Cooper JD, Bailey R, Field S, Burren O, Smink LJ, Guja C, Ionescu-Tirgoviste C, Widmer B, Dunger DB, Savage DA, Walker NM, Clayton DG, Todd JA (2006) A genome-wide association study of nonsynonymous SNPs identifies a type 1 diabetes locus in the interferon-induced helicase (IFIH1) region. Nat Genet 38:617–619 Tanaka S, Nishida Y, Aida K, Maruyama T, Shimada A, Suzuki M, Shimura H, Takizawa S, Takahashi M, Akiyama D, Arai-Yamashita S, Furuya F, Kawaguchi A, Kaneshige M, Katoh R, Endo T, Kobayashi T (2009) Enterovirus infection, CXC chemokine ligand 10 (CXCL10), and CXCR3 circuit: a mechanism of accelerated beta-cell failure in fulminant type 1 diabetes. Diabetes 58:2285–2291 Tauriainen S, Oikarinen M, Keim J, Oikarinen S, Hyöty H, group ns (2009) Detection of enterovirus in pancreatic tissues of cadaver organ donors—results from nPOD study. In: Annual meeting of Immunology of Diabetes Society, Malmö, Sweden Tracy S, Drescher KM (2007) Coxsackievirus infections and NOD mice: relevant models of protection from, and induction of, type 1 diabetes. Ann N Y Acad Sci 1103:143–151 Viskari H, Ludvigsson J, Uibo R, Salur L, Marciulionyte D, Hermann R, Soltesz G, Fuchtenbusch M, Ziegler AG, Kondrashova A, Romanov A, Knip M, Hyoty H (2004) Relationship between the incidence of type 1 diabetes and enterovirus infections in different European populations: results from the EPIVIR project. J Med Virol 72:610–617 Viskari H, Ludvigsson J, Uibo R, Salur L, Marciulionyte D, Hermann R, Soltesz G, Fuchtenbusch M, Ziegler AG, Kondrashova A, Romanov A, Kaplan B, Laron Z, Koskela P, Vesikari T, Huhtala H, Knip M, Hyoty H (2005) Relationship between the incidence of type 1 diabetes and maternal enterovirus antibodies: time trends and geographical variation. Diabetologia 48:1280–1287 Viskari HR, Koskela P, Lonnrot M, Luonuansuu S, Reunanen A, Baer M, Hyoty H (2000) Can enterovirus infections explain the increasing incidence of type 1 diabetes? Diabetes Care 23:414–416 Viskari HR, Roivainen M, Reunanen A, Pitkaniemi J, Sadeharju K, Koskela P, Hovi T, Leinikki P, Vilja P, Tuomilehto J, Hyoty H (2002) Maternal first-trimester enterovirus infection and future risk of type 1 diabetes in the exposed fetus. Diabetes 51:2568–2571 von Herrath M (2009) Diabetes: a virus-gene collaboration. Nature 459:518–519 Woodruff JF (1980) Viral myocarditis. A review. Am J Pathol 101:425–484 Yin H, Berg AK, Tuvemo T, Frisk G (2002) Enterovirus RNA is found in peripheral blood mononuclear cells in a majority of type 1 diabetic children at onset. Diabetes 51:1964–1971 Yin H, Berg AK, Westman J, Hellerstrom C, Frisk G (2002) Complete nucleotide sequence of a Coxsackievirus B-4 strain capable of establishing persistent infection in human pancreatic islet cells: effects on insulin release, proinsulin synthesis, and cell morphology. J Med Virol 68:544–557 Ylipaasto P, Klingel K, Lindberg AM, Otonkoski T, Kandolf R, Hovi T, Roivainen M (2004) Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet beta cells. Diabetologia 47:225–239 Yoon JW, Austin M, Onodera T, Notkins AL (1979) Isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N Engl J Med 300:1173–1179 Yoon JW, Notkins AL (1983) Virus-induced diabetes in mice. Metabolism 32:37–40